Analysis of Respiratory Sinus Arrhythmia and Directed Information Flow between Brain and Body Indicate Different Management Strategies of fMRI-Related Anxiety

Abstract

Background: Respiratory sinus arrhythmia (RSA) denotes decrease of cardiac beat-to-beat intervals (RRI) during inspiration and RRI increase during expiration, but an inverse pattern (termed negative RSA) was also found in healthy humans with elevated anxiety. It was detected using wave-by-wave analysis of cardiorespiratory rhythms and was considered to reflect a strategy of anxiety management involving the activation of a neural pacemaker. Results were consistent with slow breathing, but contained uncertainty at normal breathing rates (0.2–0.4 Hz). Objectives and methods: We combined wave-by-wave analysis and directed information flow analysis to obtain information on anxiety management at higher breathing rates. We analyzed cardiorespiratory rhythms and blood oxygen level-dependent (BOLD) signals from the brainstem and cortex in 10 healthy fMRI participants with elevated anxiety. Results: Three subjects with slow respiratory, RRI, and neural BOLD oscillations showed 57 ± 26% negative RSA and significant anxiety reduction by 54 ± 9%. Six participants with breathing rate of ~0.3 Hz showed 41 ± 16% negative RSA and weaker anxiety reduction. They presented significant information flow from RRI to respiration and from the middle frontal cortex to the brainstem, which may result from respiration-entrained brain oscillations, indicating another anxiety management strategy. Conclusion: The two analytical approaches applied here indicate at least two different anxiety management strategies in healthy subjects.

Scan-associated anxiety (scanxiety): the enigma of emotional breathing oscillations at 0.32 Hz (19 bpm)

“…In fact, negative RSA (nRSA; Rassler et al, 2018 , 2022 ) refers to the condition where increased state anxiety induces a complete reversal of the phase relationship between respiration and cardiac activity where the HR decreases during inspiration and increases during expiration. During nRSA, phase coupling analysis showed a reduced dominance of the respiratory rhythm over the RRI rhythm (see also Figure 1 ), and DTF revealed a significant information flow from RRI to respiration ( Rassler et al, 2023 ).…”

“…A few participants displayed an increase in anxiety at the end of the sessions similar to a study reported by Chapman et al (2010) . (ii) Participants with relatively high anxiety in the first but also in a few of the last resting states displayed a high percentage of emotional breathing oscillations around 0.32 Hz ± 0.03 ( Rassler et al, 2023 ). In six subjects, eBR of about 0.32 Hz was dominant in 63–97% of the resting state epoch.…”

“…This “BOLD avalanche effect” during nasal respiration is documented by the significant difference ( p < 0.001) between large downwards projections from the MFG to respiration (color blue, Figure 2A ) and small upward projections from respiratory centers to the cortex (color red, Figure 2A ). Note, in this case of nasal breathing, the cardiac RRI component acts as driving force for respiration in the high frequency band ( Rassler et al, 2023 ). In the case of missing respiration-entrained oscillations in the PFC, no significant differences (no BOLD avalanche effect) between the MFG outflow and respiration inflow were found ( Figure 2B ).…”

“…The blue color shows the flow from the signal marked below the given column to the signal marked at the left, and the red color the flow from the signal marked at left to the signal marked below. Significant differences between couplings of inflow and outflow are marked by stars ( p < 0.05; modified from Rassler et al, 2023 ). (B) Directed coupling without respiratory-entrained oscillations in MFG from a single subject with dominant spontaneous respiration at 0.22 Hz.…”

“…Therefore, a study in healthy subjects without any former MRI experience with scanning periods over a number of resting states was performed ( Pfurtscheller et al, 2018 ). One important point of this study was a focus on the dynamics of the anxiety level with habituation effects, and the “switch-off” of respiratory sinus arrhythmia (RSA) also known as negative RSA ( Rassler et al, 2018 , 2023 ). Another point was the investigation of the information flow (directed coupling) between brain and body in the high frequency band (0.2–0.4 Hz) close to the enhanced BR of 19 bpm (corresponds to 0.32 Hz) reported in patients ( Dziuda et al, 2019 ).…”